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Environmental Contaminant Exposure and Effects on Bats: Studies in Sichuan Province, China and Colorado, U.S.A

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Environmental Contaminant Exposure and Effects on Bats: Studies in Sichuan Province, China and Colorado, U.S.A University of Northern Colorado Scholarship & Creative Works @ Digital UNC Dissertations Student Research 5-5-2017 Environmental Contaminant Exposure and Effects on Bats: Studies in Sichuan Province, China and Colorado, U.S.A. Laura Heiker Follow this and additional works at: https://digscholarship.unco.edu/dissertations Recommended Citation Heiker, Laura, "Environmental Contaminant Exposure and Effects on Bats: Studies in Sichuan Province, China and Colorado, U.S.A." (2017). Dissertations. 405. https://digscholarship.unco.edu/dissertations/405 This Text is brought to you for free and open access by the Student Research at Scholarship & Creative Works @ Digital UNC. It has been accepted for inclusion in Dissertations by an authorized administrator of Scholarship & Creative Works @ Digital UNC. For more information, please contact [email protected]. © 2017 LAURA HEIKER ALL RIGHTS RESERVED UNIVERSITY OF NORTHERN COLORADO Greeley, Colorado The Graduate School ENVIRONMENTAL CONTAMINANT EXPOSURE AND EFFECTS ON BATS: STUDIES IN SICHUAN PROVINCE, CHINA AND COLORADO, U.S.A. A Dissertation Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy Laura Heiker College of Natural and Health Sciences School of Biological Sciences Biological Education May 2017 This Dissertation by: Laura Heiker Entitled: Environmental Contaminant Exposure and Effects on Bats: Studies in Sichuan Province, China and Colorado, U.S.A. has been approved as meeting the requirements for the Degree of Doctor of Philosophy in College of Natural and Health Sciences in School of Biological Sciences, Program of Biological Education Accepted by the Doctoral Committee _______________________________________________________ Dr. Rick Adams, Ph.D., Research Advisor _______________________________________________________ Dr. Lauryn Benedict, Ph.D., Committee Member _______________________________________________________ Dr. Scott Franklin, Ph.D., Committee Member _______________________________________________________ Dr. Thomas O’Shea, Ph.D., Committee Member _______________________________________________________ Dr. David Diggs, Ph.D., Faculty Representative Date of Dissertation Defense ________24 Feb. 2017_____________ Accepted by the Graduate School ________________________________________________________ Linda L. Black, Ed.D. Associate Provost and Dean Graduate School and International Admission ABSTRACT Heiker, Laura. Environmental Contaminant Exposure and Effects on Bats: Studies in Sichuan Province, China and Colorado, U.S.A. Published Doctor of Philosophy dissertation, University of Northern Colorado, 2017. As the world’s only flying mammals, bats fill an important ecological role in most ecosystems, acting as agents of seed dispersal, pollination, fertilization, and insect control. The human-mediated release of environmental contaminants has been implicated in the decline of many bat populations over the past few decades. Given bats’ ecological significance, I studied how bat presence and activity related to contaminated food and water sources in two global regions: 1) in and around the growing urban city of Chengdu, the capital of Sichuan Province, China, and 2) along the eastern slope of the Rocky Mountains in Colorado, U.S.A., which has been subject to 150 years of mining. In China (Chapter II), I tested mercury concentrations in fur and organochlorine concentrations in guano to assess their relationships to land use type and bat species, relative age, body condition, and phonic type. Because the Japanese pipistrelle (Pipistrellus abramus) had the highest fur mercury concentrations of bats sampled, in Chapter III I examined genetic identity and gene flow to confirm that all bats sampled were indeed P. abramus and to better understand local movements and potential implications of the contaminant concentrations. Finally, in Colorado (Chapter IV), I tested whether bat activity and feeding attempts differed locally above streams of high versus low metal contamination at high-elevation sites (>2,900 m). In China (Chapter II), iii total mercury concentrations were significantly higher in adult P. abramus than in adult Chinese noctules (Nyctalus plancyi) (P < 0.001), and significantly higher in adult N. plancyi relative to juveniles (P < 0.001). There was no significant difference in concentrations by land use type (urban versus suburban), but 57% of adult pipistrelles had fur mercury concentrations above the threshold for reduced homeostatic control, with the maximum (33 ppm) from an adult female in an agricultural area. There was no relationship between fur mercury concentration and bat body condition for either species. Hexachlorobenzene, alpha-chlordane, p,p’-DDE, o,p’-DDD, and p,p’-DDD were detected in guano but at levels well below those associated with harm. More bat phonic types were detected at a forested mountain site than agricultural or urban areas, though this could not be related to contaminant concentrations. In Chapter III, mitochondrial (cyt b) and nuclear studies confirmed that all individuals assumed to be P. abramus matched the species genetically and that there was weak population structure in Chengdu. This corroborated high gene flow in the area and a likely home range size of <10 km. Additionally, the P. abramus population had two mitochondrial clades, which may indicate ancient lineage separation due to glaciation and potential differences in susceptibility to physiological stresses. In Colorado (Chapter IV), there was no significant difference between the number of calls recorded at more contaminated sites and that at less contaminated sites. Though not statistically significant, the majority of feeding buzzes occurred above cleaner streams, suggesting that contamination could be an issue in habitats where fresh water is less available. Limited sample size and a short sampling period were constraints in all studies. iv Key words: bats, mercury, organochlorines, China, Colorado, cytochrome b, aquatic- terrestrial subsidies, Pipistrellus abramus v ACKNOWLEDGMENTS I first want to thank my friends and colleagues within the UNC Biological Sciences Department. In particular, Anna Schwabe and family, Randi Lupardus, Nadje Najar, Tom McCabe, and Lucas Dowers have provided endless personal and professional support throughout the years. Love you all. Thanks to my committee members for their patience and flexibility. To my advisor, Rick Adams, I am grateful for the support and resources you provided for me to explore uncharted territory in China and the world of ecotoxicology. Lauryn Benedict, in addition to helping me on my project, you were an amazing teaching mentor. Scott Franklin, I appreciated your knowledge of statistics and ecology, and David Diggs, you introduced me to the world of GIS. (I now feel like my life would not be complete without attending the ESRI conference in San Diego!) Last, but definitely not least, Tom O’Shea, I am grateful for you sharing your knowledge of bat ecotoxicology. You have been a huge service to the field and a source of inspiration. I am indebted to a large number of people in Chengdu without whom the foundation for this project would have been impossible. Sarah Bexell, your compassion for animals and years of pioneering conservation work in Chengdu are unparalleled. You gave me everything a visiting researcher could ask for in a foreign country. Professor Tang Ya provided me with a visa and invaluable in-country support. I am grateful to Hongyan Shi for sharing her knowledge of Chinese bats and providing access to the vi Nyctalus plancyi colony at Xi Hua Normal. Feng Rui Xi, Deng Rui, and Du Li Li, thank you for your excellent field skills, patient translations, and friendship. In addition to those in China, Kelsey Gonzales provided intrepid field support, a sense of adventure, and company overseas. Claire Ramos of Colorado State University, Pueblo made the bat fur mercury analysis possible. I owe the third chapter of this dissertation to molecular ecology gurus Mitchell McGlaughlin, Anna Schwabe, Brandee Wills, and Nathan Redecker. You went above and beyond helping me in the lab. I dedicate my fourth chapter to colleagues at USGS Fort Collins: Travis Schmidt, Johanna Kraus, and Holly Rogers, who were so gracious in sharing their knowledge and resources for the Mineral Belt project. Field support was also provided by Alex Wharry and Jenn Moore. Monetary support was provided by the UNC Biological Sciences Department, the UNC Graduate School Association, Bat Conservation International, the Colorado Mountain Club, the Explorers Club, the Audubon Society of Greater Denver, and Luo Lan and Wang Ji Shan. Thanks to all the bats that “donated” their tissues. It must have been scary, but I hope my work serves to help your future generations. Finally, this dissertation would not have been possible without the love and support of my family and my beautiful dog, Maya. Thanks for seeing me through to the end. vii TABLE OF CONTENTS CHAPTER I. INTRODUCTION……………………………………………………….........1 Background……………………………………………………………………1 Project Objectives……………………………………………………………..3 II. BAT CONTAMINANT EXPOSURE IN AN URBAN LANDSCAPE, CHENGDU, CHINA…………………………………………………….........5 Background and Significance………………………………………………....5 Methods……………………………………………………………….……...14 Results………………………………………………………………………..31 Discussion……………………………………………………………………54 III. GENE FLOW AND GENETIC DIVERSITY OF THE JAPANESE PIPISTRELLE (PIPISTRELLUS ABRAMUS) IN CHENGDU, CHINA……68 Background and Significance………………………………………………..68
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